Hostname: page-component-78c5997874-lj6df Total loading time: 0 Render date: 2024-11-10T13:30:27.111Z Has data issue: false hasContentIssue false

Panic disorder: from respiration to the homeostatic brain

Published online by Cambridge University Press:  24 June 2014

Giampaolo Perna*
Affiliation:
Anxiety Disorders Clinical and Research Unit, Istituto Scientifico H. San Raffaele, Vita-Salute University, Milan, Italy
Daniela Caldirola
Affiliation:
Anxiety Disorders Clinical and Research Unit, Istituto Scientifico H. San Raffaele, Vita-Salute University, Milan, Italy
Laura Bellodi
Affiliation:
Anxiety Disorders Clinical and Research Unit, Istituto Scientifico H. San Raffaele, Vita-Salute University, Milan, Italy
*
Giampaolo Perna MD PhD, Anxiety Disorders Clinical and Research Unit, Istituto Scientifico H. San Raffaele, Vita-Salute University, 20 Via Stamira d'Ancona, 20127, Milan, Italy. Tel.(39)-02-26433211; Fax: (39)-02 26433265. E-mail: perna.giampaolo@hsr.it

Abstract

There is some experimental evidence to support the existence of a connection between panic and respiration. However, only recent studies investigating the complexity of respiratory physiology have revealed consistent irregularities in respiratory pattern, suggesting that these abnormalities might be a vulnerability factor to panic attacks. The source of the high irregularity observed, together with unpleasant respiratory sensations in patients with panic disorder (PD), is still unclear and different underlying mechanisms might be hypothesized. It could be the result of compensatory responses to abnormal respiratory inputs or an intrinsic deranged activity in the brainstem network shaping the respiratory rhythm. Moreover, since basic physiological functions in the organism are strictly interrelated, with reciprocal modulations and abnormalities in cardiac and balance system function having been described in PD, the respiratory findings might arise from perturbations of these other basic systems or a more general dysfunction of the homeostatic brain. Phylogenetically ancient brain circuits process physiological perceptions/sensations linked to homeostatic functions, such as respiration, and the parabrachial nucleus might filter and integrate interoceptive information from the basic homeostatic functions. These physiological processes take place continuously and subconsciously and only occasionally do they pervade the conscious awareness as ‘primal emotions’. Panic attacks could be the expression of primal emotion arising from an abnormal modulation of the respiratory/homeostatic functions.

Type
Review Article
Copyright
Copyright © 2004 Blackwell Munksgaard

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Bellodi, L, Perna, G.The Panic Respiration Connection. Milan, Italy: Medical Media, 1998. Google Scholar
Griez, E, Perna, G.Anxiety and respiration. In: Davidson, JR, Nutt, D, eds. Anxiety Disorders. Oxford, UK: Blackwell Science Ltd, 2003. Google Scholar
Freud, S.The Justification for Detaching from Neurasthenia a Particular Syndrome: the Anxiety Neurosis (1894). Collected Papers. London: Hogart Press 1950: 76127. Google Scholar
Anderson, DJ, Noyes, R Jr, Crowe, RR.A comparison of panic disorder and generalized anxiety disorder. Am J Psychiatry 1984;141: 572575.Google ScholarPubMed
Ley, R.Agoraphobia, the panic attack and the hyperventilation syndrome. Behav Res Ther 1985;23: 7981.CrossRefGoogle ScholarPubMed
Klein, DF.False suffocation alarms, spontaneous panics, and related conditions. An integrative hypothesis. Arch General Psychiatry 1993;50: 306317. CrossRefGoogle ScholarPubMed
Garssen, B, Van Veenendaal, W, Bloemink, R.Agoraphobia and the hyperventilation syndrome. Behav Res Ther 1983;21: 643649.CrossRefGoogle ScholarPubMed
Cowley, DS, Roy-Byrne, PP.Hyperventilation and panic disorder. Am J Med 1987;83: 929937.CrossRefGoogle ScholarPubMed
de Ruiter, C, Garssen, B, Rijken, H, Kraaimaat, F.The hyperventilation syndrome in panic disorder, agoraphobia and generalized anxiety disorder. Behav Res Ther 1989;27: 447452.CrossRefGoogle ScholarPubMed
Gorman, JM, Askanazi, J, Liebowitz, MRet al. Response to hyperventilation in a group of patients with panic disorder. Am J Psychiatry 1984;141: 857861.Google Scholar
Griez, E, Zandbergen, J, Lousberg, H, Van Den Hout, M.Effects of low pulmonary CO2 on panic anxiety. Compr Psychiatry 1988;29: 490497.CrossRefGoogle ScholarPubMed
Antony, MM, Brown, TA, Barlow, DH.Response to hyperventilation and 5.5% CO2 inhalation of subjects with types of specific phobia, panic disorder, or no mental disorder. Am J Psychiatry 1997;154: 10891095.Google ScholarPubMed
Liebowitz, MR, Gorman, JM, Fyer, AJet al. Lactate provocation of panic attacks. II. Biochemical and physiological findings. Arch General Psychiatry 1985;42: 709719. CrossRefGoogle ScholarPubMed
Gorman, JM, Liebowitz, MR, Fyer, AJ, Fyer, MR, Klein, DF.Possible respiratory abnormalities in panic disorder. Psychopharmacol Bull 1986;22: 797801.Google ScholarPubMed
van Den Hout, MA, Hoekstra, R, Arntz, A, Christiaanse, M, Ranschaert, W, Schouten, E.Hyperventilation is not diagnostically specific to panic patients. Psychosom Med 1992;54: 182191.CrossRefGoogle Scholar
Gorman, JM, Papp, LA, Coplan, JDet al. Anxiogenic effects of CO2 and hyperventilation in patients with panic disorder. Am J Psychiatry 1994;151: 547553.Google ScholarPubMed
Zandbergen, J, Lousberg, Hh, Pols, H, De Loof, C, Griez, EJ.Hypercarbia versus hypocarbia in panic disorder. J Affect Disord 1990;18: 7581.CrossRefGoogle ScholarPubMed
Gorman, JM, Papp, LA, Martinez, Jet al. High-dose carbon dioxide challenge test in anxiety disorder patients. Biol Psychiatry 1990;28: 743757.CrossRefGoogle ScholarPubMed
Carr, RE.Panic disorder and asthma. J Asthma 1999;36: 143152.CrossRefGoogle ScholarPubMed
Perna, G, Bertani, A, Politi, E, Colombo, G, Bellodi, L.Asthma and panic attacks. Biol Psychiatry 1997;42: 625630.CrossRefGoogle ScholarPubMed
Smoller, JW, Otto, MW.Panic, dyspnea, and asthma. Curr Opin Pulm Med 1998;4: 4045.CrossRefGoogle ScholarPubMed
Davies, SJ, Jackson, PR, Ramsay, LE.Dysfunctional breathing and asthma. Panic disorder needs to be considered. Br Med J 2001;323: 631 (discussion: 631–632).CrossRefGoogle ScholarPubMed
Karajgi, B, Rifkin, A, Doddi, S, Kolli, R.The prevalence of anxiety disorders in patients with chronic obstructive pulmonary disease. Am J Psychiatry 1990;147: 200201.Google ScholarPubMed
Yellowlees, PM, Haynes, S, Potts, N, Ruffin, RE.Psychiatric morbidity in patients with life-threatening asthma: initial report of a controlled study. Med J Aust 1988;149: 246249.Google ScholarPubMed
Perna, G, Marconi, C, Battaglia, M, Bertani, A, Panzacchi, A, Bellodi, L.Subclinical impairment of lung airways in patients with panic disorder. Biol Psychiatry 1994;36: 601605.CrossRefGoogle ScholarPubMed
Spinhoven, P, Ros, M, Westgeest, A, Van der Does, AJ.The prevalence of respiratory disorders in panic disorder, major depressive disorder and V-code patients. Behav Res Ther 1994;32: 647649.CrossRefGoogle ScholarPubMed
Verburg, K, Griez, E, Meijer, J, Pols, H.Respiratory disorders as a possible predisposing factor for panic disorder. J Affect Disord 1995;33: 129134.CrossRefGoogle ScholarPubMed
Verburg, C, Perna, G, Griez, E.A case study of the 35% CO2 challenge. In: Griez, E, Faravelli, C, Nutt, D, Zohar, J, eds. Anxiety Disorders. An Introduction to Clinical Management and Research. Chichester, UK: John Wiley, 2001: 341356.Google Scholar
Beck, JG, Ohtake, PJ, Shipherd, JC.Exaggerated anxiety is not unique to CO2 in panic disorder: a comparison of hypercapnic and hypoxic challenges. J Abnorm Psychol 1999;108: 473482.CrossRefGoogle Scholar
Beck, JG, Shipherd, JC, Ohtake, P.Do panic symptom profiles influence response to a hypoxic challenge in patients with panic disorder? A preliminary report. Psychosom Med 2000;62: 678683.CrossRefGoogle ScholarPubMed
Klein, DF.Testing the suffocation false alarm theory of panic disorder. Anxiety 1994;1: 17.CrossRefGoogle ScholarPubMed
Klein, DF.Panic disorder and agoraphobia: hypothesis hothouse. J Clin Psychiatry 1996;57(Suppl. 6):2127.Google ScholarPubMed
Gorman, JM, Fyer, MR, Goetz, Ret al. Ventilatory physiology of patients with panic disorder. Arch General Psychiatry 1988;45: 3139. CrossRefGoogle ScholarPubMed
Fishman, SM, Carr, DB, Beckett, A, Rosenbaum, JF.Hypercapneic ventilatory response in patients with panic disorder before and after alprazolam treatment and in pre- and postmenstrual women. J Psychiatr Res 1994;28: 165170.CrossRefGoogle ScholarPubMed
Lousberg, H, Griez, E, Van Den Hout, MA.Carbon dioxide chemosensitivity in panic disorder. Acta Psychiatr Scand 1988;77: 214218.CrossRefGoogle ScholarPubMed
Bocola, V, Trecco, MD, Fabbrini, G, Paladini, C, Sollecito, A, Martucci, N.Antipanic effect of fluoxetine measured by CO2 challenge test. Biol Psychiatry 1998;43: 612615.CrossRefGoogle ScholarPubMed
Papp, LA, Martinez, JM, Klein, DF, Coplan, JD, Gorman, JM.Rebreathing tests in panic disorder. Biol Psychiatry 1995;38: 240245.CrossRefGoogle ScholarPubMed
Zandbergen, J, Pols, H, De Loof, C, Griez, EJ.Ventilatory response to CO2 in panic disorder. Psychiatry Res 1991;39: 1319.CrossRefGoogle ScholarPubMed
Woods, SW, Charney, DS, Loke, J, Goodman, WK, Redmond, DE Jr, , Heninger, GR.Carbon dioxide sensitivity in panic anxiety. Ventilatory and anxiogenic response to carbon dioxide in healthy subjects and patients with panic anxiety before and after alprazolam treatment. Arch General Psychiatry 1986; 43: 900909. CrossRefGoogle ScholarPubMed
Katzman, MA, Struzik, L, Vijay, N, Coonerty-Femiano, A, Mahamed, S, Duffin, J.Central and peripheral chemoreflexes in panic disorder. Psychiatry Res 2002;113(1–2):181192.CrossRefGoogle ScholarPubMed
Zandbergen, J, Strahm, M, Pols, H, Griez, EJ.Breath-holding in panic disorder. Compr Psychiatry 1992;33: 4751.CrossRefGoogle ScholarPubMed
Asmundson, GJ, Stein, MB.Triggering the false suffocation alarm in panic disorder patients by using a voluntary breath-holding procedure. Am J Psychiatry 1994;151: 264266.Google ScholarPubMed
Van der Does, WA J.Voluntary breath holding: not a suitable probe of the suffocation alarm in panic disorder. Behav Res Ther 1997;35: 779784.CrossRefGoogle Scholar
Roth, WT, Wilhelm, FH, Trabert, W.Voluntary breath holding in panic and generalized anxiety disorders. Psychosom Med 1998;60: 671679.CrossRefGoogle ScholarPubMed
Berkenbosch, A, Bovill, JG, Dahan, A, Degoed, J, Olievier, IC W.The ventilatory CO2 sensitivities from Read's rebreathing method and the steady-state method are not equal in man. J Physiol 1989;411: 367377.CrossRefGoogle Scholar
Holt, PEm Andrews, G.Hyperventilation and anxiety in panic disorder, social phobia, GAD and normal controls. Behav Res Ther 1989;27: 453460.CrossRefGoogle ScholarPubMed
Papp, LA, Klein, DF, Gorman, JM.Carbon dioxide hypersensitivity, hyperventilation, and panic disorder. Am J Psychiatry 1993;150: 11491157.Google ScholarPubMed
Maddock, RJ, Carter, CS.Hyperventilation-induced panic attacks in panic disorder with agoraphobia. Biol Psychiatry 1991;29: 843854.CrossRefGoogle ScholarPubMed
Papp, LA, Martinez, JM, Klein, DFet al. Respiratory psychophysiology of panic disorder: three respiratory challenges in 98 subjects. Am J Psychiatry 1997;154: 15571565.Google ScholarPubMed
Hegel, MT, Ferguson, RJ.Psychophysiological assessment of respiratory function in panic disorder: evidence for a hyperventilation subtype. Psychosom Med 1997; 59: 224230.CrossRefGoogle ScholarPubMed
Lum, LC.The syndrome of habitual chronic hyperventilation. In: Hill, OW, ed. Modern Trends in Psycosomatic Medicine. Saint Louis, MO, USA: Elsevier Science & Technology Books , 1976. Google Scholar
Clark, DM.A cognitive approach to panic. Behav Res Ther 1986;24: 441470. CrossRefGoogle ScholarPubMed
Holloway, W, McNally, RJ.Effects of anxiety sensitivity on the response to hyperventilation. J Abnorm Psychol 1987;96: 330334.CrossRefGoogle ScholarPubMed
McNally, RJ, Eke, M.Anxiety sensitivity, suffocation fear, and breath-holding duration as predictors of response to carbon dioxide challenge. J Abnorm Psychol 1996;105: 146149.CrossRefGoogle ScholarPubMed
Gorman, JM, Kent, JM, Sullivan, GM, Coplan, JD.Neuroanatomical hypothesis of panic disorder, revised. Am J Psychiatry 2000;157: 493505.CrossRefGoogle ScholarPubMed
Sinha, S, Papp, LA, Gorman, JM.How study of respiratory physiology aided our understanding of abnormal brain function in panic disorder. J Affect Disord 2000;61: 191200.CrossRefGoogle ScholarPubMed
Sinha, SS, Coplan, JD, Pine, DS, Martinez, JA, Klein, DF, Gorman, JM.Panic induced by carbon dioxide inhalation and lack of hypothalamic-pituitary-adrenal axis activation. Psychiatry Res 1999;86: 9398.CrossRefGoogle ScholarPubMed
Uhde, TW, Boulenger, JP, Roy-Byrne, PP, Geraci, MF, Vittone, BJ, Post, RM.Longitudinal course of panic disorder: clinical and biological considerations. Prog Neuropsychopharmacol Biol Psychiatry 1985;9: 3951.CrossRefGoogle ScholarPubMed
Coplan, JD, Goetz, R, Klein, DFet al. Plasma cortisol concentrations preceding lactate-induced panic. Psychological, biochemical, and physiological correlates. Arch General Psychiatry 1998;55: 130136. CrossRefGoogle ScholarPubMed
Abelson, JA, Weg, JG, Nesse, RM, Curtis, GC.Neuroendocrine response to laboratory panic: cognitive intervention in the doxapram model. Psychoneuroendocrinology 1996;21: 375390.CrossRefGoogle ScholarPubMed
Carr, DB, Sheehan, DV, Surman, OSet al. Neuroendocrine correlates of lactate-induced anxiety and their response to chronic alprazolam therapy. Am J Psychiatry 1986;143: 483494.Google ScholarPubMed
Hollander, E, Liebowitz, M, Gorman, J, Cohen, B, Fyer, A, Klein, DF.Cortisol and sodium lactate induced panic. Arch General Psychiatry 1989;46: 135140. CrossRefGoogle ScholarPubMed
Seier, FE, Kellner, M, Yassuridis, A, Hesse, R, Strian, F, Wiedermann, K.Automatic reactivity and hormonal secretion in lactate induced panic attacks. Am J Physiol 1997;272: H2630H2638.Google Scholar
Perna, G, Bertani, A, Caldirola, D, Di Pasquale, D, Migliarese, G, Bellodi, L.Modulation of hyperreactivity to 35% CO2 after one-week of treatment with paroxetine and reboxetine: a double-blind, randomized study. J Clin Psychopharmacology, submitted.Google Scholar
Bertani, A, Perna, G, Migliarese, Get al. Comparison of treatment with paroxetine and reboxetine in panic disorder. A randomized, single-blind study. Pharmacopsychiatry, submitted.Google Scholar
Bellodi, L, Caldirola, D, Bertani, A.Does the brain noradrenaline network mediate the effects of the CO2 challenge. J Psychopharmacology 2003;17(263–4):267268. CrossRefGoogle ScholarPubMed
Klein, DF.Response differences of spontaneous panic and fear. Arch General Psychiatry 2002;59: 567569. CrossRefGoogle ScholarPubMed
Pincus, SM.Approximate entropy as a measure of system complexity. Proc Natl Acad Sci USA 1991;88: 22972301.CrossRefGoogle ScholarPubMed
Stein, MB, Millar, TW, Larsen, DK, Kryger, Mh.Irregular breathing during sleep in patients with panic disorder. Am J Psychiatry 1995;152: 11681173.Google ScholarPubMed
Martinez, JM, Papp, LA, Coplan, JDet al. Ambulatory monitoring of respiration in anxiety. Anxiety 1996;2: 296302.Google ScholarPubMed
Bystritsky, A & Shapiro, D.Continuous physiological changes and subjective reports in panic patients: a preliminary methodological report. Biol Psychiatry 1992;32: 766777.CrossRefGoogle ScholarPubMed
Bystritsky, A, Craske, M, Maidenberg, E, Vapnik, T, Shapiro, D.Autonomic reactivity of panic patients during a CO2 inhalation procedure. Depress Anxiety 2000; 11: 1526.3.0.CO;2-W>CrossRefGoogle ScholarPubMed
Abelson, JA.Respiratory irregularity in panic patients may reflect excessive sighing. Biol Psychiatry 2000; 47(Suppl. 1):157158. CrossRefGoogle Scholar
Abelson, JL, Weg, JG, Nesse, RM, Curtis, GC.Persistent respiratory irregularity in patients with panic disorder. Biol Psychiatry 2001;49: 588595.CrossRefGoogle ScholarPubMed
Wilhelm, Fh, Trabert, W, Roth, WT.Characteristics of sighing in panic disorder. Biol Psychiatry 2001;49: 606614.CrossRefGoogle ScholarPubMed
Coryell, W, Fyer, A, Pine, D, Martinez, J, Arndt, S.Aberrant respiratory sensitivity to CO (2) as a trait of familial panic disorder. Biol Psychiatry 2001;49: 582587.CrossRefGoogle ScholarPubMed
Pine, DS, Klein, RG, Coplan, JDet al. Differential carbon dioxide sensitivity in childhood anxiety disorders and nonill comparison group. Arch General Psychiatry 2000;57: 960967. CrossRefGoogle ScholarPubMed
Pine, DS, Coplan, JD, Papp, LAet al. Ventilatory physiology of children and adolescents with anxiety disorders. Arch General Psychiatry 1998;55: 123129. CrossRefGoogle ScholarPubMed
Pincus, SM, Gladstone, IM, Ehrenkranz, RA.A regularity statistic for medical data analysis. J Clin Monit 1991;7: 335345.CrossRefGoogle ScholarPubMed
Yeragani, VK, Radhakrishna, RK, Tancer, M, Uhde, T.Nonlinear measures of respiration: respiratory irregularity and increased chaos of respiration in patients with panic disorder. Neuropsychobiology 2002;46: 111120.CrossRefGoogle ScholarPubMed
Caldirola, D, Bellodi, L, Caumo, A, Migliarese, G, Perna, G.Approximate entropy of respiratory patterns in panic disorder. Am J Psychiatry 2004;161: 7987. Google Scholar
Perna, G, Ieva, A, Caldirola, D, Bertani, A, Bellodi, L.Respiration in children at risk for panic disorder. Arch General Psychiatry 2002;59: 185186. CrossRefGoogle ScholarPubMed
Capra, F.The Web of Life. New York: Anchor Books, 1996. Google Scholar
Goldberger, AL.Non-linear dynamics for clinicians: chaos theory, fractals, and complexity at the bedside. Lancet 1996;347(9011):13121314.CrossRefGoogle ScholarPubMed
Prigogine, I.The philosophy of instability. Futures 1989;21: 396400. CrossRefGoogle Scholar
Remmers JE. Central neural control of breathing. In: Altose MD, Kawakami Y (eds). Control of Breathing in Health and Disease (Lung Biology in Health and Disease). New York: Marcel Dekker, 1999. Google Scholar
Horn, EM, Waldrop, TG.Suprapontine control of respiration. Respiration Physiol 1998;114: 201211. CrossRefGoogle ScholarPubMed
Lieske, SP, Thoby-Brisson, M, Telgkamp, P, Ramirez, JM.Reconfiguration of the neural network controlling multiple breathing patterns: eupnea, sighs and gasps. Neural Neuroscience 2000;3: 600607. Google ScholarPubMed
St-John, WM & Paton, JF R.Respiratory-modulated neuronal activities of the rostral medulla which may generate gasping. Respiratory Physiology and Neurobiology 2003;135: 97101.CrossRefGoogle ScholarPubMed
Katz, DM.Neuronal growth factors and development of respiratory control. Respiratory Physiol Neurobiol 2003;135: 155165. CrossRefGoogle ScholarPubMed
Boiten, FA, Frijda, NH, Wientjes, CJ.Emotions and respiratory patterns: review and critical analysis. Int J Psychophysiol 1994;17: 103128.CrossRefGoogle ScholarPubMed
Orem, J.The activity of late inspiratory cells during the behavioral inhibition of inspiration. Brain Res 1988;458: 224230.CrossRefGoogle ScholarPubMed
Himle, J, Thyer, BA, Fischer, DJ.Prevalence of smoking among anxious patients. Phobia Prac Res J 1988;1: 2531. Google Scholar
Breslau, N, Kilbey, M, Andreski, P.Nicotine dependence, major depression and anxiety in young adults. Arch General Psychiatry 1991;48: 10691074. CrossRefGoogle ScholarPubMed
Breslau, N, Klein, DF.Smoking and panic attacks: an epidemiologic investigation. Arch General Psychiatry 1999;56: 11411147. CrossRefGoogle ScholarPubMed
Khoo, MC.Determinants of ventilatory instability and variability. Respir Physiol 2000;122(2–3):167182.CrossRefGoogle ScholarPubMed
Ferini-Strambi, L, Spera, A, Oldani, A, Battaglia, M, Bianchi, A, Cerutti, S.Cardiac autonomic regulation during sleep in panic disorder. J Neurol Neurosurg Psychiatry 1996;61: 421422.CrossRefGoogle ScholarPubMed
Yeragani, VK, Sobolewski, E, Igel, Get al. Decreased heart-period variability in patients with panic disorder. a study of Holter ECG records. Psychiatry Res 1998; 78(1–2):8999.CrossRefGoogle ScholarPubMed
Yeragani, VK, Nadella, R, Hinze, B, Yeragani, S, Jampala, VC.Nonlinear measures of heart period variability: decreased measures of symbolic dynamics in patients with panic disorder. Depress Anxiety 2000; 12: 6777.3.0.CO;2-C>CrossRefGoogle ScholarPubMed
Radhakrishna, RK, Yeragani, VK.Decreased measures of chaos and increased nonlinearity in patients with panic disorder. Auton Neurosci 2001;88: 99108.Google Scholar
McCraty, R, Atkinson, M, Tomasino, D, Stuppy, WP.Analysis of twenty-four hour heart rate variability in patients with panic disorder. Biol Psychol 2001;56: 131150.CrossRefGoogle ScholarPubMed
Srinivasan, K, Ashok, MV, Vaz, M, Yeragani, VK.Decreased chaos of heart rate time series in children of patients with panic disorder. Depression Anxiety 2002;15: 159167. CrossRefGoogle ScholarPubMed
Yeragani, VK, Radhakrishna, KA.Non linear measures of QT interval series: novel indices of cardiac repolarization lability: MEDqthr LLEqthr. Psychiatry Res 2003;117: 177190.CrossRefGoogle Scholar
Balaban, CD.Vestibular nucleus projections to the parabrachial nucleus in rabbits: implications for vestibular influences on the autonomic nervous system. Exp Brain Res 1996;108: 367381.CrossRefGoogle ScholarPubMed
Balaban, CD, Thayer, JF.Neurological bases for balance-anxiety links. J Anxiety Disord 2001; 15(1–2):5379.CrossRefGoogle ScholarPubMed
Yardley, L, Gresty, M, Bronstein, A, Beyts, J.Changes in heart rate and respiration rate in patients with vestibular dysfunction following head movements which provoke dizziness. Biol Psychol 1998;49 (1–2):95108.CrossRefGoogle ScholarPubMed
Perna, G, Dario, A, Caldirola, D, Stefania, B, Cesarani, A, Bellodi, L.Panic disorder: the role of the balance system. J Psychiatr Res 2001;35: 279286.CrossRefGoogle ScholarPubMed
Perna, G, Alpini, D, Caldirola, D, Raponi, G, Cesarani, A, Bellodi, L.Serotonergic modulation of the balance system in panic disorder: an open study. Depression Anxiety 2003;17: 101106. CrossRefGoogle Scholar
Damasio, AR. The feeling of what happens. Body, Emotion and the Making of Consciousness. New York, NY, USA: Harcourt, 1999. Google Scholar
Parson, LM, Egan, G, Liotti, M, Brannan, S, Denton, D.Neuroimaging evidence implicating cerebellum in the experience of hypercapnia and hunger for air. Proc Natl Acad Sci 2001;98: 20412046.CrossRefGoogle Scholar
Liotti, M, Brannan, S, Egan, Get al. Brain responses associated with consciousness of breathlessness (air hunger). Proc Natl Acad Sci USA 2001;98: 20352040.CrossRefGoogle Scholar
Brannan, S, Liotti, M, Egan, Get al. Neuroimaging of cerebral activations and deactivations associated with hypercapnia and hunger for air. Proc Natl Acad Sci USA 2001;98: 20292034.CrossRefGoogle ScholarPubMed
Denton, D, Shade, R, Zamarippa, Fet al. Neuroimaging of genesis and satiation of thirst and an interoceptor-driven theory of origins of primary consciousness. Proc Natl Acad Sci USA 1999;96: 53045309.CrossRefGoogle ScholarPubMed
Herbert, H, Moga, MM, Saper, CB.Connections of the parabrachial nucleus with the nucleus of the solitary tract and the medullary reticular formation in the rat. J Comp Neurol 1990;293: 540580.CrossRefGoogle ScholarPubMed
Fulwiler, CE, Saper, CB.Subnuclear organization of the efferent connections of the parabrachial nucleus in the rat. Brain Res 1984;319: 229259.CrossRefGoogle ScholarPubMed
Shapiro, RE, Miselis, RR.The central neural connections of the area postrema of the rat. J Comp Neurol 1985;234: 344364.CrossRefGoogle ScholarPubMed
Morillo, AM, NUNEZ-ABADES, PA, Gaytan, SP, Pasaro, R.Brain stem projections by axonal collaterals to the rostral and caudal ventral respiratory group in the rat. Brain Res Bull 1995;37: 205211.CrossRefGoogle ScholarPubMed
Dobbins, EG, Feldman, JL.Brainstem network controlling descending drive to phrenic motoneurons in rat. J Comp Neurol 1994;347: 6486.CrossRefGoogle ScholarPubMed
Saleh, TM, Connell, BJ.The parabrachial nucleus mediates the decreased cardiac baroreflex sensitivity observed following short-term visceral afferent activation. Neuroscience 1998;87: 135146.CrossRefGoogle ScholarPubMed
Mutolo, D, Bongianni, F, Carfi, M, Pantaleo, T.Respiratory responses to chemical stimulation of the parabrachial nuclear complex in the rabbit. Brain Res 1998;807(1–2):182186.CrossRefGoogle ScholarPubMed